Quality Assessment of the Commercially Available Predator Amblyseius swirskii (Acari: Phytoseiidae)

Plant Health Progress 2016 17:206-210 http://dx.doi.org/10.1094/php-rs-16-0040 Plant Health Research Quality Assessment of the Commercially Available Predator Amblyseius swirskii (Acari: Phytoseiidae) Lorena Lopez, Entomology and Nematology Department, University of Florida, Gainesville 32611; and Hugh A. Smith, Gulf Coast Research and Education Center (GCREC), University of Florida, Wimauma 33598 Accepted for publication 3 September 2016. ABSTRACT Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) is a commercially available predatory mite used to control thrips, whiteflies, and broad mites in horticultural production. The inconsistent quality of mass-produced biocontrol agents is a major concern in augmentative biological control and only a few studies have tested the post-shipment quality of commercial phytoseiids. We evaluated the post-shipment quality of A. swirskii purchased from a commercial provider in the United States. Guidelines for quality control of commercially produced natural enemies, established by the International Organization for Biological Control (IOBC), were followed. Quantity, survival, fecundity, and establishment in ornamenttal peppers ( Explosive Ember ) were measured. The estimated quantity of A. swirskii motiles (immatures and adults) was quite variable among bran containers (20,968 ± 7,391 mites) but close to the number claimed in the label. Numbers of living A. swirskii females evaluated (n = 30) declined by less than 40% (26 ± 1.25 females) within two days of arrival and declined more than 50% by day eight (15 ± 1.23 females). No significant differences among days sampled were identified for female fecundity; however, fecundity varied considerably among containers. There was no population increase in the ornamental peppers during the two weeks following inoculation with A. swirskii. INTRODUCTION Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) is a predatory mite commercialized worldwide by biocontrol companies including Koppert Biological Systems (Berkel en Rodenrijs, Netherlands), BioBest Biological Systems (Leamington, Ontario, Canada), and Syngenta Bioline (Oxnard, CA) (Hunter et al. 1992; Leppla and Johnson 2010). A swirskii is use to control thrips (Thysanoptera: Thripidae), sweetpotato whiteflies (Bemisia tabaci Gennadius, Hemiptera: Aleyrodidae), and broad mites (Polyphagotarsonemus latus Banks, Acari: Tarsonemidae), and it is capable of reducing populations of two-spotted spider mites (Tetranychus urticae Koch, Acari: Tetranychidae) when alternative prey such as western flower thrips (Frankliniella occidentalis Pergande) and/or whiteflies are present in vegetable and ornamental production (Van Driesche et al. 2006; Messelink et al. 2010; Xu and Enkegaard 2010; Calvo et al. 2011; Colomer et al. 2011; Kutuk and Yigit 2011; Amor et al. 2012; Xiao et al. 2012). Releases made with poor-quality predators or made with fewer predators than needed can lead to control failures and contribute to the unpredictability of augmentative biological control (O Neil et al. 1998). The aim of quality control tests is to determine whether a natural enemy shipment arrives in a condition to properly control the pest (van Lenteren et al. 2003). Biological parameters such as survival, fecundity, sex ratio, feeding capacity, and dispersal are vital factors related to the rate of suppression provided by natural enemies over pest populations (Kim et al. 2001; van Lenteren et al. 2003). Assessments of these parameters under laboratory conditions are the first step to estimate their fitness and it is advisable to complement laboratory data with Corresponding author: Lorena Lopez. Email: lorelopezq.257@ufl.edu. doi:10.1094 / PHP-RS-16-0040 2016 The American Phytopathological Society field estimations (e.g., O Neil et al. 1998; van Lenteren et al. 2003; Hagler 2009; Park et al. 2011). The post-shipment quality has been tested mostly for commercially available parasitoids including Encarsia formosa Gahan (Hymenoptera: Aphelinidae), Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae), and insect-predator species such as Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), Hippodamia convergens Guerin (Coleoptera: Coccinellidae) (O Neil et al. 1998; van Lenteren et al. 2003), and Geocoris punctipes Say (Hemiptera: Geocoridae) (Hagler 2009). Only a few studies have tested the post-shipment quality of commercial phytoseiid species including Amblyseius cucumeris Oudemans, Amblyseius degenerans Berlese, Amblyseius californicus McGregor, and Phytoseiulus persimilis Athias-Henriot (e.g., Nicoli and Galazzi 1998; Kim et al. 2001; van Lenteren et al. 2003; Ghazy et al. 2012). These investigations were conducted to establish the standardized quality-control guidelines by the International Organization for Biological Control (IOBC) currently used worldwide for evaluation of commercially produced predatory mites (van Lenteren et al. 2003). To our knowledge, there is only one study evaluating the biological parameters of commercially available A. swirskii (Park et al. 2011). Park et al. (2011) evaluated the quality of massreared A. swirskii when fed on cattail pollen (T. latifolia L., Typhaceae) or tomato russet mites (Aculops lycopersici Massee, Acari: Eriophyidae). The authors reported similar predatory mite longevity, fecundity, and survival compared to laboratory-reared A. swirskii evaluated in similar studies (Ali and Zaher 2007; Lee and Gillespie 2011; Abou-Awad et al. 2014). Additional studies that evaluate the fitness and efficacy of commercial A. swirskii are needed to confirm the performance of this predatory mite, given that they are often shipped considerable distances before being deployed. The overall purpose of our study was to evaluate the post-shipment quality of A. swirskii purchased from a commercial provider in the United States and measure their establishment on ornamental peppers. Specific objectives were: (i) estimate the PLANT HEALTH PROGRESS DOI: 10.1094/PHP-RS-16-0040 2016, Vol. 17, No. 3 Page 206

quantity of A. swirskii motiles (immatures and adults) in purchased bran containers; (ii) assess A. swirskii female survival over an 8-day period; (iii) measure their fecundity; and (iv) evaluate the establishment and population increase of A. swirskii on Explosive Ember ornamental peppers. PLANTS AND MITES Experiments were conducted between August and November 2013 in the Vegetable Entomology Laboratory at the University of Florida s Gulf Coast Research and Education Center (GCREC), Balm, FL. The ornamental pepper Explosive Ember (Ball Horticultural Co., Chicago, IL) was used to assess the establishment of the predatory mites. Ornamental peppers were sown in cell plug trays and seedlings were transplanted (4 weeks after sowing) into 4.5-liter black plastic pots containing potting mix (Fafard 2 mix; Fafard, Agawam, MA) as growing medium with 15 g of slow-release fertilizer per plant (Osmocote 14-14-14; Scotts, Marysville, OH) in a greenhouse (25 ± 2 C, 60 ± 20% relative humidity (RH), 16/8-h light/dark photoperiod). Amblyseius swirskii individuals were purchased from Biobest (Biobest USA, Inc., McFarland, CA) a commercial provider of biological products in the United States. Predators were obtained in a bran container with a mix of thousands of predators and bran mites (Tyrophagus sp.) serving as food. A greenhouse colony of T. urticae mites was maintained on pinto bean plants (Phaseolus vulgaris L., Fabaceae) to serve as prey for A. swirskii. Tyrophagus urticae was selected to serve as prey due to its ability to develop rapidly in horticultural crops and the ease with which this species can be mass reared and handled under laboratory conditions (Hoy and Ouyang 1986; Hoy 2011). The guidelines for quality control of commercially produced natural enemies, established by the IOBC for A. cucumeris, were followed as reference to evaluate A. swirskii post-shipment quality (van Lenteren et al. 2003) due to similarity between A. cucumeris and A. swirskii with regard to prey and habitat preferences. Moreover, both predatory mites may be acquired in the same type of formulation. DATA COLLECTION Quantity estimations. Berlese funnels were used to estimate numbers of A. swirskii motiles (immatures and adults) per unit weight of bran 1 h and 2, 4, 6, and 8 days after shipment arrival. Four bran samples (1 g each) were weighed from the same container each day and poured directly into a sieve with a 12-cmdiameter, 15-cm-high, 0.40 0.45-mm mesh (LS Econet 4045; Svensson, Charlotte, NC). Each container was rotated to obtain a homogeneous mixture before taking the samples. Light bulbs (12 watts) were arranged 10 cm over the bran mix and yellow sticky cards (15 15 cm) were placed 12 cm under the sieve to trap the falling mites. All yellow sticky cards were removed 6 h later and A. swirskii motiles were counted under the stereoscope. The experiment was conducted four times; one bran container was purchased each time and stored in a cold, dark room (16 ± 1 C, 30 ± 10% RH) during the 8-day sampling period. Containers were weighed on the day of arrival and again at the conclusion of the experiment after being emptied to obtain the total weight of bran in each container. Amblyseius swirskii female survival and fecundity. To measure the survival of A. swirskii females, 30 visibly gravid A. swirskii females per bran container were assessed. Females were placed on 2.1-cm-diameter leaf discs cut from Explosive Ember leaves and placed with the abaxial side upward on water-soaked cotton (Hoy and Ouyang 1986). One A. swirskii female was placed on each disc and an excess of all stages of T. urticae was provided daily to serve as prey. Testing of females was initiated on the day the container arrived. The number of live females was recorded on a daily basis for 8 days and dead mites were removed from the leaf discs once counted. At the end of the experiments, a total of 120 A. swirskii females were evaluated under the same conditions (26 ± 1 C, 60 ± 20% RH, 16L:8D photoperiod). Fecundity of the A. swirskii females used in the survival test was measured as the number of eggs laid per female during the 8- day evaluation period. Eggs laid 24 h after the experimental setup were removed from the leaf discs and were not counted because these were produced based on the diet of bran mites included in the bran container. The number of eggs per female was recorded daily starting on the second day of evaluation. Eggs were removed from the discs once counted. Predator establishment on ornamental peppers. To evaluate the establishment of commercial A. swirskii on the ornamental pepper cultivar, 10 plants (131 ± 58 leaves per plant and 25 ± 5 flowers per plant) were inoculated 8 to 10 weeks after sowing with 1.5 g of bran (200 ± 42 predatory mites) per plant. The bran was taken directly from the container, weighed, and immediately sprinkled onto each plant. Pollen offered by the flowers present in the ornamental peppers were used as food source for the predatory mites. Two weeks after inoculation, all plants were cut into small pieces (stem and foliage) and put directly into separate metal funnels (28-cm diameter, 30-cm height, mesh width 1 mm 2 ). Light bulbs (12 watts) were placed 12 cm over the plant material and yellow sticky cards (15 15 cm) were put under the funnels to trap the falling mites. Twelve hours after the set-up, all sticky cards were removed and A. swirskii motiles on the sticky cards were counted. This process was performed four times at different dates for a total of 40 ornamental plants assessed. A single bran container was purchased each time and predators were used on the day of arrival. STATISTICAL ANALYSIS The average number of A. swirskii motiles recorded in the bran on the day of arrival and the total weight of bran were used to estimate the total number of predators per container. In order to estimate the numbers of A. swirskii motiles present in the bran samples over time (four 1-g bran samples taken each day), data were tested for normality and analyzed using analysis of variance (ANOVA) for repeated measures. No transformation was required to normalize data. Regarding female survival and fecundity data, a two-way ANOVA was performed for each set of data to identify differences among days sampled and containers. Tukey s mean separation test was carried out when appropriate. A survival analysis was performed to identify differences among the percentage of surviving females within the 8-day evaluation period. Direct counts were used to determine the number of A. swirskii establishing on the ornamental peppers. Data were analyzed using SAS 9.3, 2011 (SAS Institute Inc., Cary, NC) and Statistix 9, 2008 (Analytical Software, Tallahassee, FL). AMBLYSEIUS SWIRSKII QUANTITY ESTIMATIONS Containers acquired were received on the date promised by the company and in optimal condition. Data from the four bran containers sampled (total weight of bran, total number of predators per container, and density of predators per 1-g samples of bran) were pooled and the average weight of bran on the day of arrival (day 0) was 162 ± 23 g per container. The estimated quantity of A. swirskii motiles on the day of arrival was quite variable among containers (20,968 ± 3,360 mites) but overall PLANT HEALTH PROGRESS DOI: 10.1094/PHP-RS-16-0040 2016, Vol. 17, No. 3 Page 207

close to the number claimed in the label (25,000 A. swirskii mites). Container 4 showed the highest (25,812 ± 3,360 mites) estimated numbers of A. swirskii and only container 2 was estimated to contain unacceptable low numbers of predators (11,030 ± 3,360 mites) on the day of arrival. Survival of A. swirskii motiles over the 8-day evaluation period and among containers was highly variable (Fig. 1). The mean number of living A. swirskii motiles was 130.4 ± 42 mites per gram of bran on the day of arrival. Numbers declined to one-half (65.6 ± 41 mites) 2 days after arrival. Eight days after container s arrival the average number of mites recovered was 43.3 ± 15 mites, one-third of the number of predatory mites recovered on day 0. There was a significant day-after-arrival by container interaction for A. swirskii numbers (F 12,45 = 10.52, P < 0.0001). Predatory mite numbers were significantly higher on the day of arrival for containers 1, 3, and 4 (Fig. 1). A. swirskii abundance in containers 1 and 3 declined substantially within two days and were approximately three times lower on day eight compared to the day of arrival. Numbers of A. swirskii recorded in container 4 declined gradually within the 8-day sampling period (Fig. 1) and showed the highest numbers among containers on days 2, 4, 6 and 8. The lowest A. swirskii abundance observed on day 0 were obtained from container 2 (Fig. 1). For the formulation used in the present study, instructions are to use A. swirskii containers within two days of arrival. Our results support this recommendation. Immediate use after arrival is optimal. Bran mites served as food for the predatory mites; however, they were rarely observed by day four. Due to the scarcity of food on days six and eight, A. swirskii consisted mostly of stunted nymphs and larvae, some were dead, deformed, or unable to molt successfully. Some individuals displayed cannibalistic behavior. Additionally, the technical sheet from the commercial provider indicates that predatory mites can remain in optimal conditions up to one week if they are stored in a cold (15 C), dark room. Although the containers used in our experiments were stored under those conditions, predatory mite densities continued to decline substantially over time. Similar findings have been reported by Luczynski et al. (2008) for product-control procedures tested on P. persimilis. They exposed mass-produced P. persimilis to 5 C or 10 C for 0, 6, 12, or 18 days to determine the influence of cold on their survival following storage. Their results showed that numbers of live predators markedly declined as the length of storage increased at the two temperatures mentioned above, thus the proportion of surviving predators did not meet IOBC guidelines. Research assessing the quality of commercial A. californicus reported contrasting results (Ghazy et al. 2012). Ghazy et al. (2012) stored A. californicus females individually for 15, 30, 45, 60, or 75 days at 5.0 ± 0.3 C and 99 ± 0.1% RH under continuous darkness. At the end of the storage period, 94 to 100% of females survived when the storage period was equal or less than 30 days, but percent survival decreased with longer storage. Our results demonstrated that cold storage longer than two days after container s arrival was detrimental for A. swirskii. FEMALE SURVIVAL AND FECUNDITY No significant differences among bran containers were identified for the numbers of live A. swirskii females in the survival test. Thus, data from all containers were pooled. Significant differences were identified within the eight-day sampling period for the number of live females (F 6,18 = 12.63, P < 0.0001). The number of A. swirskii females declined gradually over time (Fig. 2A). Numbers of live A. swirskii females on day two (26 ± 1.25 mites) were approximately twice as high as day eight (15 ± 1.23 mites). No significant differences were revealed through survival analysis (df = 2, P 0.71), indicating that the rate at which A. swirskii females declined was the same each day (10% or 3 ± 0.11 fewer females per day) for each container (Fig. 2A). There were significant differences among bran containers with regard to fecundity of A. swirskii females tested (F 3, 18 = 28.73, P < 0.0001). On average, a single female oviposited 0.44 ± 0.02 eggs per day and 3.1 ± 2.2 eggs over eight days, across containers. Fecundity per day recorded from females in container 2 (0.69 ± 0.03 eggs per female) was 10 times higher compared to container 4 (0.07 ± 0.03 eggs per female, Fig. 2B). Accordingly, containers 2 and 4 showed the highest and lowest fecundity per day, respectively. No significant differences over time were identified for fecundity of A. swirskii females. Under optimal conditions (25 to 32 C and 70 to 85% RH), fecundity may vary based on the predator s diet (e.g., prey vs. pollen), and nutrient level may vary among types of prey (Carrillo et al. 2010; Messelink et al. 2010). A. swirskii females reared on P. latus produced on average 0.5 ± 0.04 (Onzo et al. 2012) or 1 ± 0.06 eggs per day (Van Maanen et al. 2010). A study evaluating the parameters of wild A. swirskii reported on average 0.92 and 0.99 eggs per female per day when fed with immature stages of western flower thrips and onion thrips (Thrips tabaci Lindeman), respectively, at 25 ± 1 C and 70% RH (Wimmer et al. 2008). Ali and Zaher (2007) reported that a single A. swirskii female fed on eggs and immature stages of the two-spotted spider mite laid 0.5-0.6 eggs per day. Even though this reported fecundity seems low, it is higher than fecundity data recorded in the present study. FIGURE 1 Mean number (± SEM) of A. swirskii motiles (immatures and adults) trapped on yellow sticky cards from four 1-g bran samples per bran container (four containers randomly designated as container 1, 2, 3, and 4) at 1 h and 2, 4, 6, and 8 days after arrival. Lowercase letters above bars indicate significant differences (P < 0.05) calculated using Tukey s mean separation test. PLANT HEALTH PROGRESS DOI: 10.1094/PHP-RS-16-0040 2016, Vol. 17, No. 3 Page 208

ESTABLISHMENT OF AMBLYSEIUS SWIRSKII ON ORNAMENTAL PLANTS Only 8.5% (17.2 ± 6.3) of the predatory mites applied to each pepper plant (200 ± 42 predatory mites on 1.5 g of bran) were recovered two weeks after inoculation (Table 1). Despite the availability of pollen in the ornamental plants, there was no population increase during the two weeks following inoculation. Our results are not consistent with the findings of Xiao et al. (2012) and Avery et al. (2014). They evaluated the survival of A. swirskii on three cultivars of ornamental peppers, including Explosive Ember, over an eight-week period. They conducted weekly monitoring and destructive leaf sampling to estimate egg and adult densities of A. swirskii per cultivar. They successfully established reproducing A. swirskii populations on Explosive Ember pepper in the post-bloom stage and recommended this ornamental pepper cultivar as optimal host for A. swirskii. They obtained around 200 predatory mites per ornamental plant two weeks after inoculation with 15 gravid females and pollen as the only food source. In the present study, the establishment evaluation was conducted under similar environmental conditions (25 ± 2 C, 60 ± 20 RH%, and 16L:8D photoperiod), ornamental pepper plants were approximately the same age (8 to 10 weeks after old) and had essentially the same average number of flowers (25 ± 5) per plant as in the investigations of Xiao et al. (2012) and Avery et al. (2014). However, in our study, this phytoseiid did not remain on, or build up on, the pepper plants by the same time period. Low numbers of A. swirskii recorded may be related to the predators fitness and the short sampling period. CONCLUSIONS All bran containers failed to meet the IOBC referenced standard of 80% survival over five days (van Lenteren et al. 2003). Our results demonstrated that A. swirskii numbers declined substantially (by approximately 50%) within two days after container s arrival. Similarly, A. swirskii females from all containers failed to meet the referenced IOBC standards of seven eggs per female over seven days (van Lenteren et al. 2003). The average fecundity observed in the A. swirskii females tested was quite low across containers and days sampled. In our study, A. swirskii female s fecundity was lower than reported in previous studies conducted under the same environmental conditions. Although A. swirskii failed to meet the IOBC standard for A. cucumeris, it may not be biologically realistic for all species of Amblyseius. A set of evaluation standards specific to A. swirskii are necessary. The responsibility for the quality control of commercially available natural enemies depends on the producers and distributors of these products. Customers need to have confidence in the viability and health of the biological control agents that they purchase to be part of their pest management programs. Thus, the evaluation of the quality of natural enemies should be conducted periodically and according to a set protocol (Kim et al. 2001). Even though there are no standard guidelines for quality control of A. swirskii yet, there are quality control procedures established for other generalist phytoseiids commercially available such as A. cucumeris that may be followed as reference. Further productcontrol investigations including other types of A. swirskii formulations (e.g., sachets and slow release packages) and comparative assessments including different commercial providers are recommended to optimize their use. Additionally, standardized methods for establishing, maintaining, and implementing rearing units are essential. ACKNOWLEDGMENTS We are grateful to Dr. Marjorie A. Hoy and Dr. Ronald D. Cave for their support during the development of the study. We thank Laurie Chambers for assistance in rearing the mites and growing the pepper plants; and James Colee and Emmanuel A. Torres Quezada for their assistance in the statistical analyses. This research was supported in part by the University of Florida s Gulf Coast Research and Education Research, Dean s Matching Assistantship Program for stipend and tuition support. TABLE 1 Direct counts of A. swirskii motiles (immatures and adults) trapped on yellow sticky cards from ornamental peppers (n = 40) inoculated with 1.5 g of bran mix two weeks prior to sampling with Berlese funnels. Mean number (± SEM) per container are included. FIGURE 2 Survival and fecundity (± SEM) of commercially available A. swirskii. (A) Survival percentage of females from all bran containers over an eightday evaluation period. (B) Fecundity measured as the number of eggs oviposited per female obtained from four bran containers (container 1, 2, 3, and 4) per day. Plant no. Container 1 2 3 4 Mean 1 1 9 72 62 2 57 30 1 21 3 6 58 15 2 4 8 2 48 7 5 15 65 3 5 6 4 5 5 12 7 1 4 9 1 8 6 74 11 2 9 4 2 1 11 10 28 2 15 3 Mean 13 ± 5.52 25.1 ± 9.31 18 ± 7.41 12.6 ± 5.38 17.2 ± 2.91 PLANT HEALTH PROGRESS DOI: 10.1094/PHP-RS-16-0040 2016, Vol. 17, No. 3 Page 209

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